Zoo Biology 29 : 237–255 (2010)
How Should the Psychological
Well-Being of Zoo Elephants be
Objectively Investigated?
Georgia J. Mason
1
and Jake S. Veasey
2
1
Canada Research Chair in Animal Welfare, Animal Science Department,
University of Guelph, Guelph, Ontario, Canada
2
Department of Animal Management and Conservation, Woburn Safari Park,
Woburn, Bedfordshire, United Kingdom
Animal welfare (sometimes termed ‘‘well-being’’) is about feelings – states such as
‘‘suffering’’ or ‘‘contentment’’ that we can infer but cannot measure directly.
Welfare indices have been developed from two main sources: studies of suffering
humans, and of research animals deliberately subjected to challenges known to
affect emotional state. We briefly review the resulting indices here, and discuss
how well they are understood for elephants, since objective welfare assessment
should play a central role in evidence-based elephant management. We cover
behavioral and cognitive responses (approach/avoidance; intention, redirected
and displacement activities; vigilance/startle; warning signals; cognitive biases,
apathy and depression-like changes; stereotypic behavior); physiological
responses (sympathetic responses; corticosteroid output – often assayed non-
invasively via urine, feces or even hair; other aspects of HPA function, e.g.
adrenal hypertrophy); and the potential negative effects of prolonged stress on
reproduction (e.g. reduced gametogenesis; low libido; elevated still-birth rates;
poor maternal care) and health (e.g. poor wound-healing; enhanced disease rates;
shortened lifespans). The best validated, most used welfare indices for elephants
are corticosteroid outputs and stereotypic behavior. Indices suggested as valid,
partially validated, and/or validated but not yet applied within zoos include:
measures of preference/avoidance; displacement movements; vocal/postural
signals of affective (emotional) state; startle/vigilance; apathy; salivary and
urinary epinephrine; female acyclity; infant mortality rates; skin/foot infections;
Published online 9 June 2009 in Wiley InterScience (www.interscience.wiley.com).
DOI 10.1002/zoo.20256
Received 8 August 2008; Revised 21 April 2009; Accepted 5 May 2009
Grant sponsor: NSERC.
Correspondence to: Georgia J. Mason, Canada Research Chair in Animal Welfare, Animal Science
Department, University of Guelph, Guelph, Ontario, Canada N1G 2W1. E-mail: gmason@uoguelph.ca
rr
2009 Wiley-Liss, Inc.
cardio-vascular disease; and premature adult death. Potentially useful indices that
have not yet attracted any validation work in elephants include: operant
responding and place preference tests; intention and vacuum movements; fear/
stress pheromone release; cognitive biases; heart rate, pupil dilation and blood
pressure; corticosteroid assay from hair, especially tail-hairs (to access endocrine
events up to a year ago); adrenal hypertrophy; male infertility; prolactinemia; and
immunological changes. Zoo Biol 29:237–255, 2010.
r 2009 Wiley-Liss, Inc.
Keywords: preference; motivation; cortisol; stress; welfare; zoos
INTRODUCTION
Ensuring the well being of zoo elephants is challenging in terms of husbandry,
cost and public perception. Objectively quantifying elephant welfare also represents
a considerable challenge. Here, we review how welfare is assessed scientifically, via
behavioral and physiological variables validated and well-used in farm and
laboratory animals. We discuss what is known about them for elephants, and
consider the work yet needed to improve the objective assessment of elephant
welfare. A companion paper [Mason and Veasey, submitted, this volume ] reviews the
few studies that have used these indices in a way that helps evaluate the population-
level well being of zoo elephants.
WHAT DO WE MEAN BY WELFARE?
Welfare relates to an animal’s affective (colloquially, ‘‘emotional’’) state: what
it feels. Our use of this word is equivalent to the term ‘‘well-being’’ [see e.g. Brown
et al., 2008], as we use these inter-changeably in this paper. Good welfare means
experiencing positive emotional states, while poor welfare involves severe or
prolonged suffering [e.g., Dawkins, 1990; Mason and Mendl, 1993; Brown et al.,
2008]. Clarifying what welfare is not helps augment this definition. First, health and
welfare are not equivalent; welfare can affect health, as reviewed below and poor
health can also affect welfare, if it involves pain or nausea. However, health issues
without such effects (e.g., a tumor the anima l cannot feel; a latent, quiescent virus; or
a potentially painful condition treated effectively with analgesics) do not affect
welfare, at least at that time. Second, welfare is not about simple genetic fitness.
While poor welfare can decrease reproductive output (as reviewed below), this is not
always the case: it would be incorrect, for instance, to assume that all farmed
livestock have good welfare simply if reproducing productively. Third, good well-
being is not about mimicking all aspects of natural life. Performing certain natural
activities may be important, but others may be relinquished harmlessly when human
provisioning and protection render them obsolete [e.g., Veasey et al., 1996a,b].
Fourth, welfare does not necessarily correspond to the intentions of the animal’s
human carers: captive animals can have good welfare despite indifferent keepers, or
poor welfare despite keepers caring deeply. Finally, death must be differentiated
from well-being. How and why death occurs is relevant to welfare, since this may
involve suffering (see below). Howeve r, loss of life per se does not imply poor
welfare: death involves the cessation of brain activity, rendering suff ering impossible;
death can also be humane (the aim of ‘‘eut hanasia’’).
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Zoo Biology
If welfare is about how animals feel, then in the absence of a common
language, how do we investigate it objectively? Subjective experiences and feelings
are inaccessible (the so-called ‘‘Other Minds’’ problem), so to assess them we use
indirect indicators. When evaluating welfare in other humans, we use both learne d
language and innate signals (smiling, crying, etc.), whose affective correlates we
understand from our own experiences. These indices generally serve us well.
However, they can be challenging or unreliable in nonverbal humans like babies or
the profoundly disabled: such cases may require measuring heart-rate or other
physiological changes validated (as discussed below) as indices of affect. When
evaluating well-being in other species, even greater challenges occur: reading alien
signals (ear-flapping, growling, etc. ); assessing physiological changes without
inducing handling/sampling stress; distinguishing valence (the positive/negative
nature of emotions, central to well-being) from mere arousal (alertness and activity,
which can increase in positive as well as negative situations); and last but not least,
interpreting all findings without anthropomorphism, bias or circular reasoning.
Certainty about conscious experiences in other animals is thus impossible; and so-
called ‘‘welfare measures’’ are merely indices from which we make only inferences.
But what are these indices and where do they originate? Most come from two
well-established fields:
1. Clinical research in humans with physical or mental problems: Ver bal reports from
suffering people (enduring stressful events like war, divorce, or bereavement;
suffering from emotional disorders such as anxiety and depression; or
experiencing physical harm that causes pain or nausea) are compared with
changes in biological functioning (e.g., cognitive changes, hormonal profiles, or
immunological changes), to yield potential biological correlates of affective state.
2. Animal-based physiology and neuroscience research: To investigate human clinical
conditions (e.g. anxiety and depression), laboratory animals are deliberately
exposed to events believed to cause stress, fear, sickness, or pain, and/or have
such suffering experimentally mitigated via analgesic or anxiolytic drugs.
Behavioral and physiological changes again yield candidate indices of the
affective states induced/redressed by these treatments.
Both these fields tend to yield similar indices, providing a range of potential
tools, as reviewed next, for assessing animal well-being.
HOW TO ASSESS ELEPHANT WELFARE?
Here, we summarize key welfare indice s, especially those sensitive to
psychological well-being (stress, frustration, and anxiety/fear), as detailed in many
stress and welfare texts [e.g., Archer, 1979; Dawkins, 1980, 1990; Mason and Mendl,
1993; Broom and Johnson, 1993; Toates, 1997; Clubb and Mason, 2002, p. 7; Brown
et al., 2008; further references are given below where they refer to additional
specifics]. We cover behavioral and psychological changes (A), then physiological
changes (B), and, finally, the consequences of physiological changes for reproduction
and health (C). We also review species-specific research on these indices in elephants.
Our aim is to evaluate the usefulness of various indices for asses sing zoo elephant
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welfare, recommend how best to use them in practice, and highlight potentially
valuable indices that have been overlooked.
Behavioral and Psychological Changes
Behavioral changes and the underlying CNS processes (e.g., appraisal,
decision-making, and learning) are central to welfare assessment because often
inherently related to pleasure, fear, and other feelings.
Preference and avoidance
Stimuli or events that decrease welfare are typically avoided, while stimuli or
events that increa se welfare are typically sought out. This can occur via unlearned
responses (e.g., approach), or learned ones such as performing an arbitrary operant
task (e.g., lever-pressing) or moving to specific locations associated with reward
(‘‘conditioned place preference’’). The more important a resource, the more effort is
generally devoted to gaining it: thus animals typically work harder (travel farther,
overcome greater obstacles, lever-press faster, etc.) for food and water than for non-
essential resources, especially when deprived. Such behavioral responses are
intimately related to the value of different stimuli and experiences: many argue
that the very functions of emotions are to control motivation (goal-directed, effortful
aspects of behavior) and promote learning [e.g., reviewed by Dawkins, 1990].
Preference tests have thus often been used to reveal what animals choose for
improved well- being. For example, chickens prefer larger cages with a sub strate to
smaller cages with wire floors [Dawkins, 1983], while naturally semi-aquatic
American mink will push door-weights as heavy as those they will push to gain
food, to reach wat er in which they can swim and ‘‘head-dip’’ [Mason et al., 2001].
Negative stimuli can be evaluated too; for example, the avoidance of potentially
noxious gasses can be assessed [Cooper et al., 1998; Jones et al., 2003], while the
aversiveness of pain to lame poultry has been revealed by their selection of food
dosed with analgesics over unadulterated food [e.g., Danbury et al., 2000]. Thus,
investigating whether stimuli or experiences induce learning, and qua ntifying the
efforts animals make to reach or avoid them, can be very useful for identifying and
ranking their affective valence.
Issues to be aware of when applying such techniques include animals requiring
time to experience and learn about the positive or negative effects of the stimuli on
offer. In addition, preference data may need interpretation: threatening stimuli can
occasionally elicit approach because of the need to gain information about potential
danger (e.g., ‘‘predator inspect ion’’ by prey species); and, furthermore, when animals
interact with a rewarding resource, the stimuli elicited by it (its sounds, odors, etc.)
and experience gained by interacting with it, may enhance or even create a
motivation for it—without such effects, ‘‘out of sight’’ could well have been ‘‘out of
mind.’’ Thus, preference for environmental enrichments, say, reveals the benefits of
adding them to an enclosure and the welfare implications of removing them once
they have been enjoyed, but does not prove that animals that have never experienced
such enrichments are suffering [Warburton and Mason, 2003].
Preference and avoidance measures are likely very useful for elephant welfare
assessment. Studies of wild African elephants’ ranging behavior certainly reveal
clustering around important resources like water [Chamaille
´
-Jammes et al., 2008],
and the avoidance of potential threats or wastes of energy. Thus, they show
240 Mason and Veasey
Zoo Biology
avoidance of roads [e.g. Blake et al., 2008] and of other areas or signs of human
disturbance [Slotow, 2002; Blom et al., 2004]; they avoid walking uphill [Wall et al.,
2006; Edkins et al., 2008; see Limin and Li, 2005 for similar findings for Asian
elephants]; and they flee from the sounds of enraged bees [King et al., 2007], from
hunts [Burke et al., 2008], and even from the odors of ethnic grou ps, Masai, who
sometimes kill them [Bates et al., 2007; the sight of distinctive red Masai clothing, in
contrast, elicits approach and attack]. In zoos, however, studies of preference or
avoidance have been little used as yet [Mellor et al., 2007 give one preliminary
example], but they could potentially be very valuable. For example, place preference
paradigms could be used to investigate whether elephants dislike being shackled at
night, whether they find some keeper contact rewarding (perhaps even the odors/
clothes of keepers with different handling styles could be presented), and to address
many other topical welfare issues. In addition, operant approaches could be used to
evaluate potential positive and negative experiences and their importance to zoo
elephants. If slopes are avoided, perhaps ramps of varying steepness could also be
used as experimentally imposed nonoperant costs, to assess efforts elephants are
prepared to make to reach/avoid different resources or stimuli [Schulte et al., 2007
review some other non-operant barriers or obstacles that could potentially allow
evaluation of motivations to approach/retreat].
Other behavioral measures related to preference, avoidance and other motivations
Tendencies to avoid threatening stimuli can be used in a quite different way in
welfare assessment. For one, avoidance responses (e.g., ‘‘startle’’) can be valuable for
assessing state, not just for quantifying the aversiveness of particular stimuli, since
increased tenden cies to avoid novel, standardized threats reflect increased underlying
anxiety. These we review in detail in the following section. (Decreasing tendencies to
avoid familiar, repeated stressors may in contrast indicate ‘‘learned helplessness:’’ see
‘‘Apathy and depression-like changes,’’ below.) In addition, frustrated motivations
(e.g. thwarted desires to approach or avoid stimuli or to engage in other activities)
can cause other behavioral responses useful in welfare assessment: ‘‘intention
movements,’’ where animals attempt to reach a relevant resource despite repeated
failure; ‘‘redirected’’ and ‘‘vacuum’’ activities, where inappropriate stimuli are used
as outlets for motivation (e.g., mating with inanimate objects); and ‘‘displacement
activities,’’ where a conflict between two incompatible motivations induces irrelevant
activities like grooming. These responses can thus help reveal an animal’s affective
state. Furthermore, if repeated and sustained, these movements can potentially give
rise to stereotypic behaviors—abnormal behaviors reviewed in more detail below.
Free-living African elephants certainly seem to display distinctive displacement
activities [reviewed and illustrated in Poole and Granli, 2009]. In an ambivalent,
slightly apprehensive animal, apparently unsure of what action to take, these include
trunk-twisting (the trunk-tip being twisted back and forth), foot-swinging (raising
and tentatively intermittently swinging the foreleg, or occasionally the hind leg), and
‘‘touch face’’ (touching the trunk to the animal’s own face, mouth, tusk, or temporal
gland). Displacement grooming and displacement feeding also occur, activities
characterized by situational and functional inappropriateness. For instance, caught
between two incompatible motivations (e.g. fleeing and fighting), wild African
241Welfare Indices for Elephants
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